Genomic analysis reveals depression due to both individual and maternal inbreeding in a free-living mammal population.

Camillo Bérénos,Jill G Pilkington,Josephine M Pemberton,Philip A Ellis

doi:10.1111/mec.13681

Abstract

There is ample evidence for inbreeding depression manifested as a reduction in fitness or fitness‐related traits in the focal individual. In many organisms, fitness is not only affected by genes carried by the individual, but also by genes carried by their parents, for example if receiving parental care. While maternal effects have been described in many systems, the extent to which inbreeding affects fitness directly through the focal individual, or indirectly through the inbreeding coefficients of its parents, has rarely been examined jointly. The Soay sheep study population is an excellent system in which to test for both effects, as lambs receive extended maternal care. Here, we tested for both maternal and individual inbreeding depression in three fitness‐related traits (birthweight and weight and hindleg length at 4 months of age) and three fitness components (first‐year survival, adult annual survival and annual breeding success), using either pedigree‐derived inbreeding or genomic estimators calculated using ~37 000 SNP markers. We found evidence for inbreeding depression in 4‐month hindleg and weight, first‐year survival in males, and annual survival and breeding success in adults. Maternal inbreeding was found to depress both birthweight and 4‐month weight. We detected more instances of significant inbreeding depression using genomic estimators than the pedigree, which is partly explained through the increased sample sizes available. In conclusion, our results highlight that cross‐generational inbreeding effects warrant further exploration in species with parental care and that modern genomic tools can be used successfully instead of, or alongside, pedigrees in natural populations.

Highlights

Inbreeding depression, the reduction in fitness or fitness-related trait values as a result of mating between related individuals, has intrigued evolutionary biologists for many decades
We examined the effects of inbreeding on first-year survival and two annualized fitness components for sheep surviving past age 1
We examined the effects of inbreeding on firstyear survival annual survival, AS, and annual breeding success, ABS

Summary

Introduction

Inbreeding depression, the reduction in fitness or fitness-related trait values as a result of mating between related individuals, has intrigued evolutionary biologists for many decades. The. While there is ample evidence for inbreeding depression, as it has been documented in a wide range of plant and animal taxa (Keller 1998; Szulkin et al 2007; Grueber et al 2010; Laws et al 2010; Walling et al 2011; Benesh et al 2014), much of the evidence is generated in controlled environments using experimental crosses or comes from self-fertilizing plants (Weller et al 2005). Much less evidence for inbreeding depression exists in wild populations with naturally occurring inbreeding, especially in vertebrates, and several ideas have been put forward to explain this relative deficiency (Keller & Waller 2002). Inbreeding might be relatively rare in natural populations, and second, sample sizes are too small to contain a sufficient number of highly inbred individuals to detect inbreeding depression (Csillery et al 2006). The calculation of inbreeding coefficients (F) requires pedigrees, which are laborious to obtain and even with genetic support, are often incomplete and contain errors, the net result of which is an underestimate of individual inbreeding coefficients (Pemberton 2004, 2008)

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